An experimental test of whether pied flycatchers choose the best ...

Current Zoology

61 (4): 604–613, 2015

An experimental test of whether pied flycatchers choose the best territory for rearing the young Elina MÄNTYLÄ1,2*, Päivi M. SIRKIÄ1, Tero KLEMOLA1, Toni LAAKSONEN1 1 2

Section of Ecology, Department of Biology, University of Turku, FI-20014 Turku, Finland Institute of Biology, Freie Universität Berlin, Haderslebener Str. 9, DE-12163 Berlin, Germany

Abstract It is often assumed that birds are able to choose a breeding territory that will later on have the most food for nestlings. Studies on this essential question are, however, few. We studied territory choice of a long-distance migrant, the pied flycatcher Ficedula hypoleuca in southwestern Finland. In one study area, we monitored the territory choice of males via the order of territory settlement. Female territory choice was studied experimentally in another study area where the correlation between male and territory quality was removed by not allowing males a free choice of territory. We defined several habitat characteristics and estimated the abundances of invertebrate prey from air, ground and trees with appropriate traps from the surroundings of the nest sites in both study areas. Against the expectation that parent birds would choose an arthropod-rich territory, neither males nor females seemed to choose those territories that later had the most food for nestlings. There was, however, some evidence that more eggs were laid in territories with more aphids and that more fledglings were produced in territories with high ant abundance. Our findings thus suggest that while it would be beneficial for birds to be able to choose food-rich territories, they may not be able to detect the right cues for doing so early in the breeding season. The possibility and importance of detecting the territories with the best prospects of rearing young may, however, vary among and within seasons and more studies on this topic are clearly needed [Current Zoology 61 (4): 604–613, 2015]. Keywords

Avian breeding, Food availability, Habitat choice, Laying date, Life history, Nestling condition

Because energy demands are particularly high when nestlings are growing (e.g. Bryant and Westerterp, 1980; Wright et al., 1998), it is important for the parents to choose a territory with sufficient food availability during the nestling phase. Several studies have indeed indicated, with various species, that birds choose territories with the highest food availability (e.g. Petit and Petit, 1996; Garcia-del-Rey et al., 2009; Michel et al., 2010). Even small-scale differences among breeding territories can have effects on breeding success and fitness for birds, and thus, territory choice has been shown to be adaptive (e.g. Martin, 1993, 1998; Franklin et al., 2000; Sergio and Newton, 2003; Forstmeier and Weiss, 2004; Chalfoun and Martin, 2007). In migratory bird species, first arriving individuals are often thought to gain the best territories and thus improve breeding success relative to late-arriving individuals (e.g. Aebischer et al., 1996; Smith and Moore, 2005). Earlier arrival of males may have also other benefits, such as avoiding inbreeding or female waiting costs in possibly adverse environmental conditions (Morbey and Ydenberg, 2001). The territories are however choReceived Feb. 28, 2014; accepted Oct. 14, 2014.  Corresponding author. E-mail: [email protected] © 2015 Current Zoology

sen several weeks before the time of the highest food demand and predicting the quality of a particular territory may be difficult if direct cues for future food abundance are missing. Especially long-lived migratory birds may use as cues for a good breeding site their breeding success in the previous years (Switzer, 1993) or the presence of con- or heterospecifics (e.g. Doligez et al., 1999; Forsman et al., 2002, 2007). There may nevertheless be several physical characteristics of the environment that the birds could use for identifying good territories in the absence of previous experience or other individuals. However, the first-arriving birds may also be high-quality individuals (e.g. Lozano et al., 1996), which makes it difficult to distinguish between the effects of territory and individual on breeding success. The pied flycatcher Ficedula hypoleuca is a holenesting passerine that forages on arthropods from the air, trees and ground. They overwinter in Sub-Saharan Africa and return to Finland in May, the males some days before the females. During the breeding season most prey items are caught from the ground (von Haar-

MÄNTYLÄ E et al.: Do pied flycatchers choose the best territory for rearing the young?

tman, 1954; Silverin and Andersson, 1984). Alatalo and Alatalo (1979) found that foraging on the ground was more common in spruce forests than in pine and mixed forests, and that airborne prey was more common in the early part of the breeding season than in the late stages of breeding. Adult birds and older nestlings consume larger and harder arthropods than younger nestlings (Silverin and Andersson, 1984). Ants, beetles and aphids were the most common food sources of adult pied flycatchers in a study by Marchetti et al. (1996). Silverin and Andersson (1984) found that ants (and other Hymenoptera) were the most common prey species delivered to the nestlings. Other common food items were spiders, caterpillars, flies, wasps and beetles. The territory choice of pied flycatchers has mainly been studied in males (e.g. Alatalo et al., 1982) and most studies on female territory choice have been unable to distinguish between the importance of territory resources from characteristics of a potential mate (Slagsvold, 1986; Lifjeld and Slagsvold, 1988). However, studies of female territory choice with experimental territory randomization among potential mates show that females may choose both territory and male quality (Alatalo et al., 1986; Sirkiä and Laaksonen, 2009). Males and females may not favor the same qualities of a territory as, for example, egg-laying and incubation are energy-demanding for females (e.g. Visser and Lessells, 2001; Nord and Nilsson, 2012), whereas the pairing period may be more demanding for males than females (e.g. Qvarnström, 1997; Buchanan et al., 2001). It is however beneficial for the fitness of both parents that food availability is high during offspring feeding. Eeva et al. (2000), for instance, found a tendency that pied flycatchers had more fledglings in years when there were more arthropods. Earlier studies have shown that pied flycatchers prefer territories in deciduous forests (e.g. Lundberg et al., 1981; Siikamäki, 1995), with low density of birches (Alatalo et al., 1986) and with high abundances of flying insects and leaf damage (Lundberg and Alatalo, 1992). Because female pied flycatchers tend to choose territories in the same order in consecutive study years (Mäntylä et al., 2010), there seem to be some stable characters in the best territories that at least the females can recognize. Furthermore, laying dates are earlier (Lundberg et al., 1981) and clutch sizes are larger in deciduous than in coniferous forests (Lundberg et al., 1981; Siikamäki, 1995). Other studies have suggested that there may be more food available in lush deciduous forests than in usually more barren coniferous forests

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(van Balen, 1973; Mänd et al., 2005; Veen et al., 2010; Burger et al., 2012). We examined whether pied flycatchers choose first those territories that will have the most food during the nestling period and subsequently the highest breeding success. To this end, we measured several environmental characters (amount and size of different types of trees, bushes and undergrowth) and estimated the abundances of potential food items (arthropods in the air, ground and trees) from several territories. Male choice of territories was studied in one study area by examining their order of settlement in potential territories, which were created by providing nest-boxes. Female choice was studied in another study area after experimentally breaking the correlation between the qualities of the territory and the male. This study measured food abundance and environmental characters of the territories during one breeding season in two forest areas where no nest-boxes had been placed before, and therefore the birds did not have previous breeding experience with the area. The reproductive success of the birds was monitored to confirm quality differences among territories and to find out whether the birds could choose the best territories for rearing the young. We predicted that if the birds are able to estimate the forthcoming food availability, both males and females would prefer territories with high food abundance during the nestling period.

1

Material and Methods

The study was conducted in two forest areas (Ruissalo and Maaria) in Turku, SW Finland (60° 27′ N, 22° 16′ E) in 2008. The distance between the study areas was approximately 20 km. Both study areas were mixed forests with the main tree species being Scots pine Pinus sylvestris and Norway spruce Picea abies, with smaller numbers of deciduous trees such as birch (Betula pendula and B. pubescens) and European aspen Populus tremula. We chose locations for the experimental territories prior to the breeding season of the pied flycatchers. The Maaria forest had 29 and the Ruissalo forest 27 territories. The minimum distance between neighboring territories was 50 m. In each territory, two nest-boxes of similar model, material and size (inside dimensions 12.5 × 12.5 cm, inside height 23.6 cm, entrance hole 32 mm) were placed on trees a maximum of 10 m from each other. We used two nest-boxes to reduce variation in nest site quality among the territories. The nest-boxes were hung at 120–140 cm height. There were no other

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nest-boxes in the forests and only few natural cavities, which we did not observe pied flycatchers using for breeding. There had not been any nest-boxes before this study in the Maaria forest and part of the Ruissalo forest was also a new nest-box area. In south-western Finland about 20% of males and 10% of females show breeding area fidelity, returning to the same area in the following year (von Haartman, 1960; Eeva et al., 2008). As our study areas were mostly new to pied flycatchers, only a few birds in the Ruissalo forest may have returned to an area that they had experienced during the previous year. Pied flycatcher males usually defend a rather small area around the nest-box (median 10 m; von Haartman, 1956), so they can breed quite close to each other, although both males and females search for food from a larger area around the territory core (von Haartman, 1956). If a great tit Parus major or blue tit Cyanistes caeruleus carried nest material to a nest-box at a territory, the particular nest-box was gradually moved off the territory core bit by bit (in total 20 m from the original position) and another empty nest-box was installed in the territory core (altogether six cases). This way each site constantly consisted of two available nest-boxes for the pied flycatchers and the experimental set-up remained as similar as possible. The study set-ups however differed between the forests because in Maaria we followed territory choice of males (hereafter male territory choice observation) and in Ruissalo that of females (hereafter female territory choice experiment). In the male territory choice observation, the nestboxes were erected in early May. At this time, the first pied flycatcher males had just arrived to southern Finland, whereas most other hole-nesting passerines (mainly tits) had already started their nesting and thus would not compete for nest-boxes anymore. The territories were checked every morning to record the arrival date of a male, which was defined as the date when a constantly singing male was documented in the territory core. Because some males were observed moving between several territories, their choice was not determined until a male remained at only one territory. In those cases, the day of the territory choice was the date when the male was first observed in that territory (i.e. the response variable used in the statistical analyses was the May date, 8–19 May). During the actual breeding time no obvious cases of polyterritoriality or polygyny were observed, but the males were not captured and therefore the paternity of the broods remained unknown. As the coloration of male pied flycatchers is highly variable (Lundberg and Alatalo, 1992), individuals could

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be identified based on black-brown dorsal coloration, and size and shape of the white forehead patch (Lundberg and Alatalo, 1992; Sirkiä, 2011). In the female territory choice experiment we used a design that randomized males to different quality territories (Alatalo et al., 1986; Sirkiä and Laaksonen, 2009). This was done in seven separate woodlands (on average approximately 3 hectares each) at a minimum distance of 300 m from each other. Within the woodlands, we established territory sites about 50 m apart from each other. In the beginning of the experiment, one territory site per woodland was drawn at random and the first nest-boxes were installed at these first random sites. The first arriving male found thus only one territory site (two nest-boxes) to occupy. The nest-box sites were checked daily in the morning and in the afternoon to monitor the arrival of the first males. As soon as a territory site was occupied by a singing male for a minimum of six hours (to make sure that the male was resident), another pair of nest-boxes was installed at the next randomly chosen territory site in the same woodland. The arriving males consequently only found a single vacant territory at any one time and they had no opportunity to choose among territories within a particular woodland. Eventually there were 2–6 occupied territories within each woodland. If an already settled male tried to take over another territory, the nest-boxes of the new territory were removed, compelling the male to return to its original territory. Some males paired during the settlement period but we prevented them from breeding by removing the nest material daily. As a preparation for the selection period, we captured the already paired females, transported them in textile bird holding bags and released them in one of two locations with free nest-boxes 33 km away from the study area. After the female removals, all males restarted singing in a few hours (see also Lundberg and Alatalo, 1992) and we started the selection period from the following day. From the following morning onwards the sites were checked twice a day to monitor the choice order of territories. A choice of territory was considered to have happened after a female had settled and started to build a nest. We measured female territory choice within a woodland by calculating a standardized rank value for each territory. A standardized value was calculated using the formula: (2 × rank – 1)/(2 × n), where rank is the original choosing order within the woodland and n is the total number of available territories occupied by singing males in that woodland (Alatalo et al., 1986). If two territories were chosen at the same time, both were as-


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radius (i.e. bushiness) and the share of deciduous trees from all trees (using the relascope data). All these environmental variables were measured by standing in the territory core (between the two nest-boxes) and turning full 360° circle around. We estimated the diameter of the territory core to be approximately 20 m. To measure the available arthropod food in each territory, we used pitfall traps, glue traps, count of aphids and estimation of missing leaf area (Table 1). With these traps and counts, we estimated the availability of different arthropods that adult pied flycatchers are known to capture for themselves and for their offspring (see Introduction). In each territory (approximately 500 m2), we had four pitfall traps (diameter 10 cm) to estimate the amount of ground arthropods and four yellow cylinder-shaped glue traps (about 300 cm2 each) to measure the amount of flying insects (in trees at 1.5 m height). The collection of arthropods lasted for two weeks and it was timed so that it covered the nestling period (14 days) surrounding the median date for breeding attempts. Due to minor variation in laying date (see above), we assumed that we caught arthropods during most of the nestling period in each territory. The pitfall and glue traps were placed approximately 10 m from the nest-boxes in the four different principal compass points. The leaf area removed (LAR) was estimated from 20–100 leaves (depending on the leaf size of the tree species) from four deciduous trees in each territory core to indicate the amount of leaf-chewing insect herbivores. From these same leaves we counted the amount of sap-sucking aphids. The LAR estimation and aphid count were done at the same time as pitfall and glue traps were brought to the territories. For statistical analyses of the amount of captured/counted arthropods, we calculated means per

signed the same rank value. The territories that were not chosen had the lowest rank in that particular group and if there were many, they all had the same value. After standardization the values ranged between 0 and 1 with an average value of 0.5. By using standardization we could compare the pairing ranks of the territories from all woodlands of the study with each other. Although the standardized rank ranging between 0 and 1 is not strictly speaking a continuous variable, it was analyzed with linear models, as the residuals of the models followed normality and this approach allowed the use of multiple explanatory variables. In both study areas, laying date (1 May = 1), clutch size, mean nestling condition (i.e. residual mass after controlling for body size of 12-day-old nestlings) and fledgling number were documented. Of the total of 29 and 27 territories (male and female territory choice, respectively), eggs were laid on 29 and 20, nestlings hatched on 28 and 19, and 27 and 19 produced at least one fledgling. No nest predation was documented. In the male territory choice area, the mean (± SE) laying date was 26.8 ± 0.58, mean egg number was 6.1 ± 0.18 (in nests where at least one egg was laid) and mean fledgling number was 5.0 ± 0.28 (in nests that produced at least one fledgling), while in the female territory choice area those numbers were 25.5 ± 0.33, 6.9 ± 0.11 and 6.1 ± 0.27, respectively. As forest habitat characteristics may be important for habitat choice (see Introduction), we recorded from all territories the forest type (barren or lush) based on undergrowth vegetation species (Cajander, 1949), the forest stand volume (m3 of wood, based on relascope point sampling, Bitterlich, 1984), the percentage of undergrowth covered with  1.0 m high bushes within a 360°

Table 1 Means, standard deviations (SD), coefficients of variation [CV%, calculated as (SD/mean) × 100], minimum values (min) and maximum values (max) of different food items and environmental variables in the male territory choice study area (left, n = 27) and in the female territory choice study area (right, n = 19) Variables

mean

SD

CV%

min

max

ants (no. of ind.)

152.8 | 326.8

232.1 | 611.6

151.9 | 187.1

6.0 | 5.8

855.0 | 1866.0

arthropods (no. of ind.)

23.2 | 16.9

11.4 | 8.9

49.2 | 52.4

7.3 | 4.8

54.8 | 41.3

leaf area removed (%)

3.1 | 3.8

1.5 | 2.0

48.7 | 52.4

0.2 | 0.3

6.3 | 7.6

aphids (no. of ind.)

7.2 | 13.5

11.4 | 12.7

158.0 | 93.7

0|0

43.0 | 52.3

flying insects (no. of ind.)

38.6 | 55.4

22.8 | 25.7

58.9 | 46.3

12.8 | 29.5

100.5 | 134.0

share of deciduous trees (%)

3.5 | 18.3

5.6 | 23.9

160.0 | 130.6

0|0

22.2 | 80.0

bushiness (%)

32.1 | 36.8

16.9 | 22.2

52.6 | 60.3

5.0 | 5.0

63.0 | 88.0

stand volume (m3)

80.3 | 135.9

42.9 | 52.7

53.4 | 38.8

22.5 | 38.5

187.0 | 217.0

forest type (barren vs. lush)*

93 % vs. 7 % | 42 % vs. 58 %

*As ‘forest type’ is a classifying variable, only percentage of barren vs. lush forest types in both study areas is shown. Values for food items are based on means per trap or per tree for each territory. For a brief description of the variables, see Table 2.

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trap or per tree for each territory. Because the female territory choice area was lusher and generally had more arthropods than the male territory choice area, the study area was used as an explanatory factor in statistical analyses of breeding success, including the response variables that were common for both study areas. To analyze the data for the effects of environmental and food variables on territory choice and breeding success, we used general linear models and an information theoretic model selection approach. For all response variables (i.e. male territory choice, female territory choice, laying date, egg number, nestling condition and fledgling number), we first defined nine alternative candidate models (and in addition a model that included only the intercept), which corresponded to direct food-related and other environmental characteristics that we considered potentially important for pied flycatchers (Table 2; as recommended by e.g. Arnold, 2010). The analyses were done with standardized values (mean = 0; SD = 1) of the quantitative explanatory variables. To find the best models, considering both fit and complexity, the candidate models were ranked according to their Akaike’s information criterion for small sample sizes, AICc (Burnham and Andersson, 2002; Johnson and Omland, 2004). Models were compared using two measures associated with the AICc: deltaAICc (ΔAICc) and Akaike weight (wi). ΔAICc is a measure of each model relative to the best model, whereas wi indicate the probability that the model is the best among the whole set of candidate models. All statistical analyses were done with SAS statistical software, version 9.2.

2

Results Prey abundance differed considerably among territo-

Table 2

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ries (Table 1). In spite of this, there was substantial model uncertainty in finding the best models among the tested candidate models for both territory choices and measures of breeding success. In all model comparisons there were several different models within two ΔAICc units and no single model was supported over all the others according to Akaike weights (Table 3). In addition, in most cases even the highly ranked models (wi > 0.90) seemed to have poor fit, as their R2 (i.e. coefficient of determination) values were relatively low (below 0.1) (Table 3). All the highest ranking models (ΔAICc = 0.00) included only one explanatory variable. The model including only the intercept provided the best fit for territory choice of both males and females (Table 3), indicating that none of the tested candidate models with food-related or environmental factors had support in the data. The highest-ranked models for clutch size and fledgling number nevertheless explained more than 20% of the variation (Table 3). Clutch sizes were largest on territories where aphids were abundant during the nestling stage (Tables 3, 4), while there was a tendency for the number of fledglings to increase with the number of ants in the territory (Tables 3, 4). There were also trends for larger clutch sizes in territories with more ants and more fledglings in territories with fewer arthropods (Table 3). A slight trend could also be seen for earlier laying date in territories with less leaf damage (LAR; Tables 3, 4).

3

Discussion

Our results suggest that neither male nor female pied flycatchers seem to choose territories that would later have the most food for nestlings, as the best model for both male and female territory choice was the null model, which included only the intercept and no expla-

Analyzed models with the explanatory variables included in the models

Model number

Variables*

Description#

1

ants, other ground arthropods, flying insects, leaf area removed, aphids

all food variables

2

forest type, stand volume, share of deciduous trees, bushiness

all environment variables

3

ants

only ants

4

other ground arthropods

arthopods, excluding ants

5

leaf area removed

LAR, leaf-chewing herbivores

6

aphids

only aphids

7

flying insects

all flying insects

8

forest type, share of deciduous trees

lushness of the forest

9

bushiness, stand volume

openness of the forest

* Forest type, with two categories, was the only categorical explanatory variable, whereas all others were continuous variables. Breeding success was measured at both study areas and thus the variable ‘study area’ was added to all analyses of breeding parameters. # Brief description of the model. Key words used to identify the models in other tables are in italics.


natory variables. This is surprising, considering that food abundance is important for growing offspring (Naef-Daenzer and Keller, 1999; Slagsvold and Wiebe, 2007). Our results nevertheless suggest that the numbers of aphids and ants in the territory core are of some importance for breeding success of the pied flycatcher. There are several possible explanations (detailed below) for why parents do not seem to be choosing the territories that have the most food available during nestling period. Firstly, reliable cues of later food availability may not exist when birds are choosing territories in spring. Secondly, food availability in other phases of breeding may be more important for territory choice than that during nestling period. Third, it may be that Table 3

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the importance of the territory core for foraging is relatively small. Fourth, it might be that sufficient amounts of food were present in all studied territories, although there was a lot of natural variation among territories in food abundances. We did find that abundance of arthropod prey was correlated with reproductive success. Finally, it is also possible that our measurements on the amounts of arthropods were not accurate enough or that we missed some important characteristics of the habitat. It may be that the parent birds are unable to detect suitable territory quality cues that would allow them to choose the best territory for feeding their young. Such cues should be reliable and predictable, and reflect environmental variation over a sufficient time (Boulinier

Differences in Akaike Information Criteria (ΔAICc) and fit (R2) for different candidate models (see Table 2) Statistic

Intercept Only

Food

Environment

Ants

Arthropods

LAR

Aphids

Flying Insects

Lushness

Openness

ΔAICc

0.00

12.66

7.44

1.65

2.44

1.54

1.80

2.50

3.31

4.71

0.000

0.073

0.126

0.029

0.002

0.032

0.024

0.000

0.063

0.017

ΔAICc

0.00

12.01

4.79

1.02

2.49

2.19

2.54

2.27

4.89

2.85

R2

0.000

0.118

0.226

0.055

0.002

0.013

0.000

0.010

0.016

0.087

Response variable

male territory choice female territory choice laying date clutch size nestling condition fledgling number

R

2

ΔAICc

1.66

8.22

8.82

2.77

2.52

0.00

2.60

2.41

4.84

3.65

R2

0.000

0.164

0.103

0.070

0.075

0.121

0.073

0.077

0.078

0.100

ΔAICc

8.90

6.02

9.86

1.68

2.62

4.12

0.00

3.62

6.46

5.35

R2

0.000

0.311

0.209

0.215

0.200

0.175

0.242

0.183

0.178

0.196

ΔAICc

1.96

10.86

3.30

0.15

0.00

0.14

0.05

0.10

0.21

1.96

R2

0.000

0.056

0.148

0.050

0.054

0.051

0.053

0.052

0.101

0.066

ΔAICc

6.66

3.86

9.39

0.00

1.47

3.95

3.92

2.64

4.40

6.14

R2

0.000

0.323

0.189

0.214

0.189

0.145

0.146

0.169

0.182

0.151

The analyses were done with standardized values (mean = 0; SD = 1) of the quantitative variables. The lowest ΔAICc values (0.00) are in bold. The underlined ΔAICc values indicate models that combine for at least 0.90 cumulative Akaike weight (wi) (i.e. there is at least 90 % chance that the best model is included).

Table 4 Parameter estimates with 95% confidence intervals (lower, upper) of the best models (i.e. ΔAICc = 0; see Table 3) and models with only the intercept or the study area Response variable male territory choice female territory choice laying date clutch size nestling condition fledgling number

Explanatory variable (model) intercept

ants

arthropods

LAR

aphids

study area*

12.45(11.21, 13.69) 0.36(0.27, 0.45) 26.27(25.50, 27.03)

0.64(-0.12, 1.41)

6.41(6.15, 6.66)

0.52(0.002, 1.05)

0.40(0.11, 0.70) 5.36(4.88, 5.84)

1.38(-0.14, 2.89)

-0.06(-0.35, 0.24) 0.41(-0.005, 0.83)

-0.75(-1.22, -0.27) 0.44(-0.15, 1.03) -1.25(-2.16, -0.33)

The analyses were done with standardized values (mean = 0; SD = 1) of the quantitative variables. *Calculation formula: ‘male territory choice area’ – ‘female territory choice area’.

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et al., 1996; Danchin et al., 2008). For example, insect eggs as cues of caterpillars later in the summer are of no use if the caterpillars hatch after the bird has left the area. Variation in spring phenology after avian territory choice and egg laying may add to the uncertainty of cues for an insect-rich territory. Although the timing of transitions from one stage of the avian breeding cycle to the next exhibits little variability, the development of invertebrate prey availability may be strongly dependent on environmental conditions (Eeva et al., 2000). There can be huge differences in arthropod population densities between years (e.g. Baltensweiler et al., 1977; Ruohomäki et al., 2000) with varying effects on passerines (Enemar et al., 2004; Hogstad, 2005). We have previously shown that pied flycatchers did not prefer territories with herbivore-damaged birches that had caterpillars hidden from view (Mäntylä et al., 2010). The importance or possibility to detect cues may, however, vary both in time, for example within and among seasons, and in space, for example among different vegetation zones, which should be taken into account in future studies. Parent birds need sufficient food during territory and mate choices, egg laying and incubation (e.g. Meijer et al., 1990; Visser and Lessells, 2001; Nord and Nilsson, 2012). In this study, we measured food availability only during the nestling period. It may, however, be that food availability during the early phases of the breeding season is more important than later during the nestling period. In our study, 80.3 % of the eggs laid produced a fledgling [average in pied flycatcher populations is approximately 70%–80 % according to Lundberg and Alatalo (1992)] and the nestling mortality was only 4.5 %. There apparently was thus no severe shortage of food during the nestling period. It may, however, be that in early May when males are defending the territory and females are laying eggs, that food availability is limited (e.g. due to earlier phenological state and colder weather). Synchrony with the caterpillar food peak is important for pied flycatchers in Central Europe (Both et al., 2010; Burger et al., 2012). In Northern Europe, pied flycatchers are less dependent on caterpillars as the food source for nestlings (Eeva et al., 2000; Burger et al., 2012). However, the amount of herbivory (i.e. explanatory variable LAR) did not affect territory choice or breeding success of pied flycatchers in our study, although for some reason females tended to lay eggs slightly earlier in territories with lower LAR. We measured the amount of arthropods and environmental characteristics only from the core of each

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territory. Selection should favor individuals that minimize parental effort by locating nest sites within prey-rich territories. (Naef-Daenzer, 2000; Stauss et al., 2005), and therefore a territory core with abundant food should be beneficial for them. This is also indicated by the result that fledgling number was higher in territories with more ants. It may, however, be that the birds are able to compensate for scarcity of food in the territory by searching for food from a larger area (von Haartman, 1956). The cost for a bird to fly a few hundred meters farther to search for food may be low compared to defending a larger territory (Huhta et al., 1999; Moreno et al., 1999). In future studies, habitat selection should be considered over a larger spatial scale, for example between different forest patches with different habitats. It is possible that our methods did not fully capture the variation in food abundance among territories, as estimation of arthropod food on whole home range scale would be very demanding. For example, not all arthropod species can be captured with static traps. Therefore, we may not have caught all species that are important for pied flycatchers, or the prey species they use as cues of territory quality. Furthermore, we did not count the number of caterpillars or collect their droppings, but relied on the LAR as indication of abundance of leafchewing herbivores, which may be a less accurate method (Hunter, 1987). In general, an individual can use current or previous-year cues from the environment and/or from intra- or interspecifics when searching for a breeding site, such as migrant pied flycatchers observing the clutch sizes of resident tits (Parus spp.) (Loukola et al., 2013). Because our study sites were mainly new breeding areas for pied flycatchers, they could only use current cues in their choices. Furthermore, predation risk may affect the territory preferences of pied flycatchers (Fontaine and Martin, 2006; Thomson et al., 2006; Morosinotto et al., 2010). However, no predation on nestlings or adults was documented in our study areas. The abundance of food items during egg laying may affect female body condition and further clutch size (Visser and Lessells, 2001). In our study, the abundance of aphids in the territory core was positively associated with the number of eggs laid. However, the importance of prey availability in the earlier breeding phases (i.e. pairing, egg-laying and incubation) for territory choice remains mostly unknown. Providing extra food to the pied flycatcher breeding territory may increase the number of fledglings (Verhulst, 1994; Siikamäki, 1998). The younger the nestlings are, the softer food they are


given (Pruska, 1980), and thus aphids are likely suitable prey items for young nestlings. Adult pied flycatchers may also eat aphids (Marchetti et al., 1996). Older nestlings are also given harder food items, such as ants (Meidell, 1961). We found that more fledglings were produced in territories with more ants, and it may be that the parents fed ants to the nestlings at our study sites. The association between breeding success and the number of ants in the territory is interesting as ants also eat small arthropods and can thus compete with insectivorous birds for food resources (e.g. Eurasian treecreepers, Certhia familiaris, have a higher breeding success in territories without ants; Aho et al., 1999). Our results do not suggest strong competition between ants and pied flycatchers, as ants seem to be important food items for these birds. Overall, contrary to earlier results (e.g. Lundberg et al., 1981; Siikamäki, 1995; Eeva et al., 2000), the measured territory characters had only a relatively weak effect on breeding success. This may suggest that the importance of territory characters depend on environmental conditions and/or that the quality of parents is more important for breeding success than the territory quality (Siikamäki, 1995; Przybylo et al., 2001; Sergio et al., 2009). It is also possible that small quality differences between the territories were not recognized by birds (Canal et al., 2012), or that many of the territories were of equal quality (Goodenough et al., 2009). It has often been assumed that early arriving birds accrue benefits over their late arriving counterparts because they are able to choose the best territories, in addition to possibly gaining more mating opportunities. Abundant food during nestling rearing is one of the obvious features of a high-quality territory. The results of our study during one breeding season indicate that while the abundances of aphids and ants correlate with breeding success, neither male nor female pied flycatchers seem to choose territories with the most food during the nestling period. In years when, for example, the weather is unfavorable during the breeding season, the result could have been different. It may be that there are no cues available for the birds early in the breeding season for making correct choices about conditions later in the breeding season or that the birds are unable to detect those cues. Acknowledgements We would like to thank city of Turku for letting us use their forests in this experiment, research assistants for their help in field and laboratory work, and David Swanson for checking the language. The study was financially supported by the Jenny and Antti Wihuri foundation

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(grant to EM), the Emil Aaltonen foundation (grant to PS and TL), the Ella and Georg Ehrnrooth foundation (grant to PS) and the Academy of Finland (decision numbers 111195 and 129143 to TK). The capture of birds was done under license LOS-2007-L-264-254 from the Regional Environment Centre of Southwestern Finland.

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